The Yellow River is the key corridor for Tamarix austromongolica to disperse from Asia inlands to east seashores

Abstract Plants of the Tamarix L. genus (Tamaricaceae) mainly occur in arid inlands of Asia, but a few species occur in the coastal areas of China, and the Yellow River may account for this. This study was conducted to elucidate whether and how the Yellow River affects the pattern and development of the Tamarix genus, involving two critical species of Tamarix austromongolica Nakai and Tamarix chinensis Lour. With geographical distribution data, relationships of T. austromongolica with the Yellow River and the pertaining watershed were examined using the method of random permutation. The base‐diameter structures of T. austromongolica populations were investigated and compared between different riparian lands that suffer discriminative water inundation. The nearest distances from T. austromongolica locations to the Yellow River and the pertaining watershed were significantly lower than the theoretical expectations in the condition of random distribution (p < .05). In many riparian lands along the Yellow River, wild T. austromongolica populations occurred with vigorous juveniles, despite frequent human disturbances. In coastal areas near the present estuary of the river, wild T. austromongolica plants were still found. In T. austromongolica populations near the Yellow River and sea, the rates of juvenile plants were significantly higher than in other populations situated farther from the river or sea. These findings suggest that the Yellow River can facilitate the eastward dispersal of Tamarix plants that reasonably caused the evolution from T. austromongolica to T. chinensis in ancient coasts in the China east.


| INTRODUC TI ON
Most species of the Tamarix L. genus (Tamaricaceae) adapt well to subtropical and temperate arid lands, playing an important role in determining ecosystem functions and services (Zhang, 2004;Zhang et al., 2001).The adaptations are inherited from the common ancestors that originated in ancient Mediterranean before the Miocene (Terrones & Juan, 2023;Zhang et al., 2001Zhang et al., , 2002)).Plants of this genus later dispersed into West and Middle Asia, East Europe, and North Africa, and developed into many lineages and species (Baum, 1978;Villar et al., 2023;Zhang et al., 2002).The Xinjiang Uygur Autonomous Region, China is a secondary distribution center for Tamarix to disperse on, and 18 species and one variety exist in China (Liu, 1994;Zhang & Zhang, 1990).Of these species, Tamarix austromongolica Nakai and Tamarix chinensis Lour.are the critical frontiers to disperse eastward for coastal areas (Liang, Liu, et al., 2019;Liang, Quan, et al., 2019;Wen et al., 2020;Zhang, 2004).
Tamarix austromongolica is a widespread shrub species in areas on and near the north-east Tibetan Plateau, from which the Yellow River originates and flows toward the East Sea.These areas include the Qinghai Province, Gansu Province, Ningxia Hui Autonomous Region, Inner Mongolia Autonomous Region, Shaanxi Province, and Shanxi Province, whereas T. chinensis occurs mostly in the eastern provinces of China, such as the Shandong, Hebei, and Jiangsu Provinces (Liang et al., 2018;Wen et al., 2020).Tamarix austromongolica was confirmed to be the closest relative to T. chinensis because T. chinensis was time-calibrated to evolve from T. austromongolica as a young species about 0.69 million years ago in the Quaternary Pleistocene, while T. austromongolica originated from another much more ancient Tamarix species at least 2.27 million years ago (Liang, Liu, et al., 2019;Liang, Quan, et al., 2019;Sun et al., 2016;Zhang, 2004).About 1.165 million years ago, the ancient Yellow River broke through the Sanmen Gorge now in Henan Province along with the profound uplift of the Tibetan Plateau (Liang et al., 2018;Pan et al., 2005;Wen et al., 2020).
After that, some T. austromongolica plants were supposed to disperse along the river to eastern coasts, where they were then selected and shaped repeatedly by the coastal environments, at last making the new species of T. chinensis (Liang et al., 2018;Zhang, 2004).Tamarix chinensis thus adapted to temperate coastal areas relatively better than T. austromongolica, and at present it has become a common species in widespread coasts around the Huanghai and Bohai seas (Li et al., 2020;Liu et al., 2023;Sun et al., 2023).In contrast, T. austromongolica is routinely absent from these areas, but mainly present in west inlands (Liang et al., 2018).
The Yellow River now enters the Bohai Sea in the Shandong Province (about 37.8° N), whereas thousands of years ago, it used to enter the Huanghai Sea at south ancient sites (about 33° N), now in the Jiangsu Province (Du et al., 2024;Xu et al., 2006;Xue et al., 2004).The current estuary of the Yellow River must not be the initial origin sites of T. chinensis, but may carry clues for retrieving the ancient origin of T. chinensis, which should be deeply related to hydrological and soil conditions more than climatic ones (Liang et al., 2018).Tamarix austromongolica and T. chinensis are very similar in morphological traits for their close phylogenetic relationship (Baum, 1978;Liang, Liu, et al., 2019;Liang, Quan, et al., 2019;Zhang, Tan, et al., 2003).Even so, careful taxonomists can clearly distinguish them through the major difference that the inflorescence rachises of T. austromongolica are rigid to keep straight or upright, but those of T. chinensis are soft to only keep droopy (Zhang & Zhang, 1990).In these contexts, the study was conducted to seek evidences that are meaningful in elucidating the initial origin of T. chinensis from T. austromongolica and the geographic role of the Yellow River in determining the historical evolution and distribution pattern of Tamarix plants in East Asia.

| Data collection
Occurring sites of T. austromongolica were cited from concerned publications (Liang et al., 2018;Wen et al., 2020).Geographic information system (GIS) shape files of the Yellow River and pertaining watershed (Figure 1 River, mainly about real occurrences, recruitment state, and human disturbances (Figure 1 and Table 1).
In July 2022, flowering T. austromongolica plants were identified and investigated in Dengkou (Inner Mongolia Autonomous Region), Yongning (Ningxia Hui Autonomous Region), Yanchi (Ningxia Hui Autonomous Region), and Dingbian (Shaanxi Province), where specialists familiar with forest distribution showed us the major occurring sites.At each site, a random walk route was used to sample 200 T. austromongolica plants appearing in sequence on the route, and the measurement item was the base diameter of these plants, including small saplings or juveniles and large adults.In contrast to other sensitive indices, the base-diameter index is relative steady and easy for measurement and evaluation (Fu et al., 2015;Fu & Shen, 2017).
Tamarix austromongolica forests were also found in coastal area near the estuary of the Yellow River, but only on a limited scale relative to T. chinensis (Wen et al., 2020).In this study, this condition was verified on the spot in August 2022, and the base diameters of T. austromongolica plants were investigated at two sites that were in low tidal flat near the sea often with moist salty soil and another evidently higher, drier coastal backland >3 km from the sea.At each site, 20 random quadrats in sizes of 10 m × 10 m were selected to measure and record the base diameters of all T. austromongolica plants occurring in the quadrats.

| Data analyses
With the cited sites, the dependences of T. austromongolica on the Yellow River and related watershed were examined using PASSaGE 2 software, where all the sites were randomly permuted for 499 times, thus calculating theoretical averages of the nearest distances from these sites to the river and watershed and correspondingly the 95% confidence intervals of the theoretical averages on the hypothesized condition of random T. austromongolica occurrence, that is, thorough independence of the river and watershed (Rosenberg & Anderson, 2011).The results were additionally verified with the spot investigation data along the river in July 2023.
In Omap Software (www.ovital.com), the nearest distances to the Yellow River were measured from the four investigated sites in Yongning, Dengkou, Yanchi, and Dingbian.Then, the base diameters of T. austromongolica plants at these sites were pairwise compared using the Wilcoxon test that works for all data, even not following the statistically normal distribution.Finally, the base diameters of T. austromongolica plants near the sea were compared between the two different sites with the T test method.These analyses were completed in R4.3.2 software (www.r-proje ct.org).

| Position relationships with the Yellow River and relevant watershed
The nearest distances from the 38 cited sites to the Yellow River averaged 0.37 degree (Table 2).Provided these sites were random, the distances would average 1.24 degree, with the 95% confidence TA B L E 1 Wild Tamarix austromongolica plants investigated along the Yellow River.2).Provided these sites were random, the distances would average 0.51 degree, with the 95% confidence interval from 0.75 degree to 0.27 degree according to the 499 times of random permutations.These results indicate that the T. austromongolica species is very likely to depend on the Yellow River for living and dispersal because the averages of the nearest distances are much lower than the corresponding 95% confidence intervals.
This opinion was also confirmed by the spot investigation along the riverbank (Table 1), where T. austromongolica plants persisted in recruiting, despite varieties of human disturbances.

| Base-diameter structures of T. austromongolica populations along the Yellow River and the seashore
The moist as the Yongning site.At these sites, the T. austromongolica populations significantly differ in their base-diameter structures (Table 3, Figure 2).At the Yongning site, the rate of juveniles is the highest because its average base-diameter is significantly smaller than those of the three other sites.Likewise, the T. austromongolica populations behave differently at the two coastal sites (Figure 3).In general, the young T. austromongolica plants are in a higher rate in the low tidal flat than in the high backland, with the base-diameter averages of 2.22 ± 0.97 cm for the tidal flat and 3.41 ± 1.24 cm for the backland (p < .001,T test).The results indicate that no matter on low tidal flat or near the Yellow River, T. austromongolica population recruits easily with rich saplings or juveniles.That is, moist lands are helpful for T. austromongolica plants in occurring.

| Dependence of T. austromongolica on the Yellow River
The occurrences of T. austromongolica populations are closely related to the Yellow River, in spite of the human disturbances, such as farming, grazing, and felling.The Yellow River must help T. austromongolica grow.Fruits of T. austromongolica are so minute as to adapt to anemochory well, instead of hydrochory, and this species inherits the capability of the Taxmix genus to be acclimated to moist, salty riparian lands similar to those in the ancient Mediterranean (Zhang, Pan, & Yin, 2003).Fruits of this species can disperse easily with convenient winds here and there.Provided dropping in moist soils, it is easy for the fruits to start new lives as saplings, juveniles, and adults.The moist lands are common beside the Yellow River.Thus, the major river makes a substantial number of moist habitats to entertain T. austromongolica for germinating and growing.This perspective is confirmed again by the further evidence that at the Yongning riparian site and another tidal flat, juveniles of T. austromongolica grow in higher rates than at other comparative sites farther from the river or sea.

| The role of the Yellow River in Tamarix genus evolution
The Yellow River is a key factor for the Tamarix genus to disperse further for east areas beside the seas.as a new species about 2.27 million years ago in the ancient reaches of the upper Yellow River, presumably near the current Jishi County, Gansu Province, and later, individuals of this species kept dispersing up and down along the river that were confined to only northwest China (Li et al., 2023;Liang, Liu, et al., 2019;Liang, Quan, et al., 2019;Wen et al., 2020).After the Yellow River broke through the Sanmen Gorge about 1.165 million years ago because of the stepwise uplift of the Tibetan Plateau and the persisting downward river erosion, the river was then conditioned to flow till the east seas (Liang et al., 2018;Liu & Sun, 2007;Pan et al., 2005).As a result, T. austromongolica plants could disperse step by step along the river, repeating the life phases of fruit dispersal with winds, fruit dropping in riparian soils, germinating, maturing, and bearing fruits again for dispersal once again.After they arrived in coastal areas, they would be selected by new environment and evolved to adapt more and more to the changed environment, finally bringing forth the new species of T. chinensis about 0.69 million years ago (Liang et al., 2018;Liang, Liu, et al., 2019;Liang, Quan, et al., 2019).Taking too many millennia, the T. chinensis species now have developed as a widespread dominant species along the lengthy coastlines beside the Bohai and Huanghai seas (Li et al., 2020;Liang, Liu, et al., 2019;Liang, Quan, et al., 2019).

| Evidences for the history from T. austromongolica to T. chinensis
The exceptional occurrence of T. austromongolica near the present Yellow River estuary is actually not an impossible odd but a living clue in retrieving the historic evolution of T. austromongolica to T. chinensis that should have completed in ancient coasts connected to the ancient Yellow River at old estuaries about 0.69 million years ago (Liang, Liu, et al., 2019;Liang, Quan, et al., 2019;Xue et al., 2004).Even now, the T. austromongolica plants still disperse along the Yellow River to the present estuary, but because of undeveloped adaptations, they are not enough to challenge the large-scale dominance of T. chinensis across lengthy broad coastal areas (Li et al., 2020;Liu et al., 2023).With massive fruit production and supply, T. austromongolica may achieve local dominance near the new estuary of the Yellow River.On this occasion, heredity carried by the T. austromongolica plants may be incorporated by T. chinensis through smooth interspecific hybridization, which is very common within the Tamarix genus, including T. austromongolica and T. chinensis (Baum, 1978;Sheidai & Koohdar, 2023;Terrones & Juan, 2023).In this case, the arriving T. austromongolica are only a complement to T. chinensis in further development and evolution, other than a challenge to T. chinensis for thriving in much broader coastal areas than now.

| CON CLUS ION
The occurrences of T. austromongolica are highly dependent on the Yellow River that provides this species with preferred habitats of riparian ) were downloaded from the Resources and Environment Scientific Data Center, Chinese Academy of Sciences (www.resdc.cn).In July 2023, wild T. austromongolica plants in blossom were investigated on the spot along the banks of the Yellow F I G U R E 1 Cited and investigated distribution sites of Tamarix austromongolica along with the Yellow River in China.The investigated sites are labeled as in Table1.The sites in Heyang and Linyi are too near to be clearly discerned, and so are the sites in Zhungaerqi and Hequ.
lands.Along the major river, T. austromongolica plants are conditioned to disperse further, and their diminutive haired fruits also facilitate the dispersal through anemochory.The living and dispersing mechanism of T. austromongolica must work not only now but also long before the Yellow River met the sea.It is believable that after the Yellow River broke through the Sanmen Gorge and succeeded in meeting the east seas, T. austromongolica successfully dispersed into coastal areas and later resulted in the origin of the advanced T. chinensis.Now, T. austromongolica plants still disperse toward the new estuary of the Yellow River, but they are not sufficient to replace T. chinensis as a widespread dominant species along lengthy coastal areas, and can only play as a vivid clue showing the ancient origin of T. chinensis from T. austromongolica.AUTH O R CO NTR I B UTI O N S Hongxiao Yang: Conceptualization (lead); formal analysis (equal); investigation (equal); writing -original draft (equal).Xinwei Liu: Conceptualization (supporting); data curation (equal); investigation (equal); writing -review and editing (equal).Honghao Gan: Investigation (equal); resources (equal).Jia Sun: Investigation (equal).Yanxia Pan: Investigation (equal).Jianmin Chu: Conceptualization F I G U R E 2 Base-diameter structures of Tamarix austromongolica populations at four sites in the Yellow River watershed.F I G U R E 3 Base-diameter structures of Tamarix austromongolica populations beside the Bohai Sea in different distances.
Tamarix austromongolica came into being The nearest distance is a composite of longitude and latitude differences from the Yellow River and pertaining watershed, instead of horizontal distances in unit of kilometer.Comparison of base-diameters of Tamarix austromongolica populations between every two sites.